Abstract
Virtually all fishes rely on flows of water to transport food to the back of their pharynx. While external flows that draw food into the mouth are well described, how intraoral waterflows manage to deposit food at the esophagus entrance remains unknown. In theory, the posteriorly moving water must, at some point, curve laterally and/or ventrally to exit through the gill slits. Such flows would eventually carry food away from the esophagus instead of toward it. This apparent paradox calls for a filtration mechanism to deviate food from the suction-feeding streamlines. To study this gap in our fundamental understanding of how fishes feed, we developed and applied a new technique to quantify three-dimensional (3D) patterns of intraoral waterflows in vivo. We combined stereoscopic high-speed X-ray videos to quantify skeletal motion (XROMM) with 3D X-ray particle tracking (XPT) of neutrally buoyant spheres of 1.4 mm in diameter. We show, for carp (Cyprinus carpio) and tilapia (Oreochromis niloticus), that water tracers displayed higher curvatures than food tracers, indicating an inertia-driven filtration. In addition, tilapia also exhibited a 'central jet' flow pattern, which aids in quickly carrying food to the pharyngeal jaw region. When the food was trapped at the branchial basket, it was resuspended and carried more centrally by periodical bidirectional waterflows, synchronized with head-bone motions. By providing a complete picture of the suction-feeding process and revealing fundamental differences in food transport mechanisms among species, this novel technique opens a new area of investigation to fully understand how most aquatic vertebrates feed.
Highlights
IntroductionHow organisms acquire food is largely determined by the medium in which they feed (Herrel et al, 2012)
As the velocity of the water tracers is calculated in reference to the entrance of the esophagus, this low velocity corresponds to the approaching speed of the fish
Compared to previously employed invasive techniques to quantify intraoral flows, such as endoscopy (Callan, 2003; Smith and Sanderson, 2008) or pressure recordings (e.g. (Van Leeuwen and Muller, 1982)), our non-invasive approach yields a more complete view of the spatial aspects of intraoral suction-feeding dynamics, allowing us to demonstrate the existence of different hydrodynamic mechanisms for food transport
Summary
IntroductionHow organisms acquire food is largely determined by the medium in which they feed (Herrel et al, 2012). Aquatic organisms commonly exploit the dense and viscous properties of water to carry food from a distance, towards and through their mouth, by generating flows of water These flows typically result from suction created by a powerful expansion of the feeding apparatus, for example, in fishes that suddenly increase the volume of their buccopharyngeal cavity (Alexander, 1969). A wide range of aquatic vertebrates across a large size range employ suction feeding: from larval fishes (Drost et al, 1988) and frog tadpoles (Deban and Olson, 2002) to whales (Werth, 2004), and some carnivorous plant with tiny suction traps (Müller et al, 2020) Because of this impressive diversity in organisms, making use of suction feeding, it plays an important role in all major aquatic habitats and feeding niches throughout the water column (Wainwright et al, 2015)
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